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Bug sex: the top five most bizarre invertebrate sexual practices

The animal kingdom can be an aggressive place when it comes to reproduction, with alpha males killing off their counterparts to ensure their genetic line persists. Invertebrates, however, present some pretty extreme competition in the stakes for the most bizzare, rapacious or unusual sexual practices.

To hunt down the weirdest of these interludes, Wired.co.uk sought out the advice of biologist, insect-lover and Wild Sex presenter Carin Bondar. In her web series Bondar approaches the subject matter with a hint of humanisation and a whole lot of humour: "I love humanising because it gives us a chance to put examples out there that grab attention," she told Wired.co.uk. "I enjoy giving them a face and a description. You might want to call it shock value, but this is all totally real -- there's a lot of kink going on, so I never get tired of talking about this stuff."

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From eyeball-grabbing to self-castration, here are Bondar's top five weirdest insect sex stories.

5. Evolutionary arms race: water striders

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Watching water striders skim and skip across a pond is surely a hypnotic sight. Watch two hop around together under a microscope, and it quickly becomes clear this dance is anything but hypnotic for the female. "In a lot of insects there's a polyandrous mating system whereby one female mates with several males," explains Bondar. "She can often get enough sperm for her entire reproductive life from very few inseminations. But of course males that haven't had a chance to make a deposit yet will want to get their sperm in there. This creates a conflict between the sexes and it's beautifully illustrated in the water strider."

This conflict has taken on the form of an evolutionary arms race -- one that might seem a beautiful example of nature's battle of the sexes, but is also a pretty horrific one for the female. As science writer Ed Yong commented when the University of Toronto recently revealed the latest terrifying nugget of information about male water strider tactics, "the worst sex you have ever had pales in comparison to what female water striders have to put up with".

Using high-speed cameras and electron microscopes, the team of evolutionary ecologists uncovered the mystery behind the male water strider's inordinately spiked antennae, which it uses to grasp and cling on to the female until she submits to its advances. "The males have evolved some very sinister grasping structures," says Bondar. "They have these very well-crafted antennae that actually grasp and clamp on to the female's eye, right around her socket so that he can get on there. It's almost like a wrench."

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In one species, the Rheumatobates rileyi, the mature male's antennae are actually lined with spikey hairs and bend back on themselves, so they literally do wrench around the eyeball and hook on.

[Html##&lt;iframe width="455" height="315" src="http://www.youtube.com/embed/DOgSIXQu06I" frameborder="0" allowfullscreen&gt;&lt;/iframe&gt;##] "They're large, muscular, and fitted with spines and spikes exquisitely adapted for grasping -- a long way from an insect feeler," said one of the University of Toronto biologists. Towards their ends, the antennae actually become singular spikes, which perfectly fit around the female's eye and use fine hairs to clamp on. The team found that the Dll gene in the male of the species had evolved to spur on antennae adaptation.

The female, however, also has a few tricks. "She has evolved several anti-grasping structures to be able to turf him off because it's a big cost for her, ecologically speaking," says Bondar. "He's not only a monkey on her back, but him being there makes her more susceptible to predators and takes more of her time away from doing things like finding food." Carrying the male on her back while she struggles to kick him off forces the female to expend 20 percent more energy. Furthermore, when the male actually manages to insert its appendage into the female, it expands so it locks on and he is harder to shake off.

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Some females have developed elongated spines to help shake off the males, but even this is not always enough. Enter the genital shield.

It was discovered in 2009 that females of the Gerris gracilicornis species can block their reproductive entry point with hard, chastity belt-style shields. Not to be scuppered, the male has come up with a shifty tactic based on blackmail. Namely, he bangs his legs on the water's surface while mounted on the female, drawing attention from predators. In the aptly named paper on the topic, "Male water striders attract predators to intimidate females into copulation", it was explained that the threat is basically, "let me have sex with you, and I'll stop making vibrations on the water's surface, which will otherwise lead to us both being swallowed by a passing fish". The female is underneath so is most likely to get eaten -- the male can just let go and flit away. "For a male his primary goal is to get his sperm into the next generation and hers is simply to choose a suitable male," says Bondar, "but in the water strider I'm not sure there is much choice going on so it really is a big conflict. It's an ongoing battle -- many more thousands of years from now I wonder what we'll see."

4. Extreme mate guarding: symbiotic isopods

Isopods, those tiny little sea bugs that dart around the intertidal zone, appear to be pretty inoffensive little creatures.

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Look to the miniscule symbiotic isopods they carry, however, and it's a whole other story. "They're almost microscopic and live entirely on the big ones," says Bondar. "Here, it's another case of males wanting to guarantee paternity." "They will grab fairly mature eggs straight from the female when the eggs have not even hatched, and as soon as they hatch they will impregnate them. It's so mean -- it's baby rape."

That would have been the sub-header of this section, but we concluded that's one humanisation of invertebrates too far. After all, as Bondar says, "this is actually a very sound strategy".

The males will patiently carry the eggs with them at all times to ensure no other competitor has the chance to get there first (the guarding element) then leave them to it once hatched and impregnated. What's remarkable about the immature females is that they can carry the male's seed for long stretches of time. "They aren't born sexually mature," explains Bondar. "The females carry the seed in them and when they become sexually mature it's already in there and it guarantees the paternity. They have sperm storage organs and certain insects can even store for several months." "You hear all sorts of these horrible stories, but this one kind of takes the cake," laughs Bondar, with more than a little glee.

3. Self-castration v. cannibalism: white widow spiders

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Many species of spider are cannibalistic -- namely, the female eats any suitor who tries to impregnate her. As such, the male of the species appears to have accepted its fate: instead of battling the inevitable, he has come up with novel methods of ensuring as much sperm gets in the female as possible. Enter the fascinating world of spider self-castration. All male spiders, including white widows, are equipped with pedipalps -- penis-like appendages that are used to penetrate the female and get the goods to the sperm storage organs. "Here, it's all part of the same desire of a male wanting to keep his sperm in there and keep other male's out," says Bondar. "With the isopods it was guarding, and for the white widow it's a type of mate-plugging." "Once he's transferred the sperm into the female's reproductive opening with his pedipalp, he will break it off." Gulp. "So now he's without a pedipalp and it's stuck in the female's opening.

It's the equivalent of a man breaking off his penis in the vagina and hoping this will be an effective barrier to any other future sperm deposits. And in the white widow it actually is. It's an effective way for him to exclude other males from making deposits into her."

According to a 2012 study, the method actually enables the male to get more sperm into the female. A team of evolutionary biologists monitored wild virgin female spiders and dissected them post-copulation to discover that the breaking of the pedipalp ensured continual sperm transfer -- even post-detachment. The biologists asserted it was an evolutionary tactic developed to counter the female's murderous tendencies and typically brief duration of copulation. "In spiders you'll see a trend of a very, very large female and a tiny male," says Bondar. "Again, as is the case with many cannibalistic species, the male has to sneak in there and be so careful." "In another species the male actually cinches his waist up and has the effect of displacing the vital organs to the outer periphery so when he rolls in there and tries to impregnate the female, she'll bite him, but because a lot of the organs have been displaced he lives through the first reproductive bout and can come back for a second."

In the case of the white widow, the male actually has a spare pedipalp, however he rarely gets the chance to use it. "The unfortunate reality for many white widow males is that he has a good chance of getting eaten right then and there," says Bondar. "Chances are it's the end of the road for them; she eats them."

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Madagascan mouse lemurs, males use a sticky substance to cover the female's vagina post-copulation. It hardens and acts as a barrier, preventing other males in the group from having a go. "Invertebrates take it to the max though," says Bondar. "Actually breaking off your reproductive appendage is pretty darn extreme. They're in it for the win."

2. Tie me up tie me down: golden orb web spiders

According to Bondar, the penchant for BDSM (bondage, domination, and sado-masochism) that was popularised by a certain novel this year has been an everyday practice among golden orb web spiders for many years -- though, in this spider's case, it's known as mate binding. "In the water striders they evolve structures to be aggressive with the female, but in spiders they can't be aggressive with her because she's just going to eat him."

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Here, the male literally binds up the female with spider silk," says Bondar. "In a 2011 study they found the males that bound up the females had a greater chance of surviving the reproductive encounter and could return for future ones. They were also able to mate for much longer, increasing their chances of successfully transferring their sperm. For a lot of these spiders timing is important, it doesn't mean much if you've been in there for 30 seconds if it takes you a minute to finish."

According to the biologists that carried out the 2011 study, the males were able to double the intimate time spent with the females. Since the process also involved binding the female over some chemoreceptors, the researchers looked into whether the mating success was down to the chemistry, or solely sensory factors. "Is he trying to mess with her perception of what she's feeling, because all of a sudden she can't feel?" asks Bondar. "Are we dealing with messing her up chemically?"

Li Daiqin, one of the paper's authors, concluded that both chemical and tactile cues are essential. However, "tactile sensation is more important -- thus we came up with the term 'mate massaging', which may be better 'mate binding'."

1. Trauma v. titillation: bedbugs and earwigs

If you thought female water striders had it bad, look away now.

While the former have developed aggressive and violent appendages used to restrain the female and increase their chances of copulation, bedbugs just go ahead and stab the female with theirs. "The males have evolved to have a very weapon-like, penis-like structure that they essentially just stab into the female," says Bondar. "It doesn't matter where -- they just pierce her body cavity and it creates a massive surface wound."

After breaching the exoskeleton the sperm rides along in the female's hemolymph fluid till it reaches her sperm storage organ. "What's interesting is what used to be the reproductive opening has completely atrophied because the male never uses it."

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The males are not too bothered about how many times they take a stab at it either, so to speak. "The strategy is always to get sperm in there regardless of her well-being because sperm is cheap, he wants to spread it out as much as he can over and over. It can lead to extreme trauma for females. In some insects males will kill her because it's too much."

Before we lose all hope in the joy of sex, Bondar has chosen to leave us with a story that relays the brighter -- and more pleasurable -- side of bug copulation.

In the insect kingdom, as in the animal kingdom, females choose their partners according to certain things -- they might be bigger, stronger, or faster. In the case of the striders, it's not about choice, but about which male is the most aggressive. Alternatively, the male might be faster, and therefore more likely to be successful. In earwigs, it's none of the above. The female goes for the male with the biggest reproductive member, a genetic characteristic. "This is perplexing because of the characteristics I outlined," says Bondar. "They're not bigger, they're not stronger and they're slower because with a longer appendage it takes him a lot longer to get his sperm in there. All these things are not lining up, and yet females are lining up to have sex with them." "So biologists have literally concluded that the tactile stimulation the females are receiving is what keeps them coming back for more. They just liked it."